Metazoan embryonic development relies on precise cellular and morphogenetic processes, which are highly-energy intensive. Mitochondria, the powerhouse of the cell, play vital roles in various such morphogenetic events for instance, epithelial to mesenchymal transitions, cell migration, and tissue remodeling. Regulation of mitochondrial morphology and activity is essential for embryonic survival in C. elegans, Drosophila, zebrafish and mice. Asymmetric mitochondrial activity and distribution within the embryo has been shown to govern embryonic axis specification in Xenopus, sea urchin and Drosophila. Mitochondria are fragmented and dispersed in early Drosophila blastoderm embryos, and they migrate apically during cell formation (cellularization) in all the cells throughout the embryo. We have characterized the mitochondrial organization and its function during Drosophila gastrulation. We observe that a second mitochondrial migration takes place, from the basal side to the apical side of the cells, which is specific to the ventral furrow. The mitochondrial migration in the ventral furrow is found to be microtubule-dependent and is regulated by the Dorsal/Nfkb signaling pathway. Mitochondria need to be fragmented for migration, as loss of mitochondrial fission protein, Dynamin related protein 1 (Drp1), prevents the apical migration and causes mitochondrial clustering in the basal regions of the cell. Drp1 mutant embryos (Drp1SG) show reduced Myosin II levels at the apical side of ventral furrow cells resulting in a broader ventral furrow. Proteomic analysis of mitochondria isolated from Drp1SG embryos reveals decreased levels of respiratory chain complexes suggesting that the clustered mitochondria in Drp1 mutant embryos are functionally inactive. Whole mRNA sequencing coupled with proteomic analysis indicate normal expression of Dorso-ventral patterning genes but an upregulation of antioxidant pathways in Drp1SG embryos. A decrease in reactive oxygen species (ROS) is confirmed by reduced fluorescence of the dye, dihydroethidium (DHE). Strikingly, additional depletion of mitochondrial ROS scavengers and mitochondrial fusion machinery in Drp1SG embryos results in mitochondrial fragmentation rescuing the defects in mitochondrial migration and ventral furrow formation. Our findings reveal a novel Dorsal/NF-kB-dependent regulation of mitochondrial migration and a critical role of mitochondrial fission and activity in early embryonic development. Our study provides a framework for understanding how disruptions in mitochondrial fission and ROS balance may contribute to mitochondrial disorders where defects in cellular movement and architecture are common hallmarks.